In line with the growing interest in humans' nutrition, production of microalgae-based functional foods characterized by an increased content of bioactive substances is attractive. The aim of this study was to investigate the potential of microalgae as additives to feed for laying hens, to enrich the eggs with polyunsaturated fatty acids (PUFA) and selenium/carotenoid antioxidants. Our results showed that supplementation of hens by feed containing 1% of Trachydiscus minutus or 1% of Japonochytrium marinum leads to increase of long-chain PUFA in eggs by 26-66%. Addition of 1% of Scenedesmus obliquus to feed causes the increase of lutein and cantaxanthin in eggs by 48% and 18%, respectively, and addition of 0.5% selenium enriched Chlorella vulgaris increases the final content of organic selenium in eggs by 100-152%. As concerns selenium, it is important to notice that its bioavailability has to be considered. Despite the higher concentration of total selenium in Vischeria helvetica than in C. vulgaris, its bioaccessibility in Vischeria was limited, thus out of usage for feeding purposes. Administration of combinations of selenium enriched Chlorella + Japonochytrium and Chlorella + Schizochitrium verified the increased concentrations of organic selenium, PUFA, as well as carotenoids, with no adverse effect on quality and productivity of eggs. The study confirmed the potential of both traditional as well as new microalgae to be used as feed supplements for functional eggs production. The supplementation of hens by specific microalgae combinations could be advantageous in terms of spectrum of bioactive compounds present.

Department of Food Analysis and Nutrition University of Chemistry and Technology Prague Technická 3 166 28 Prague Czech Republic

EcoFuel Laboratories s r o Ocelářská 9 190 00 Praha 9 Czech Republic

RABBIT Trhový Štěpánov a s Sokolská 302 257 63 Trhový Štěpánov Czech Republic

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Alagawany M, Elnesr SS, Farag MR, Abd El-Hack ME, Khafaga AF, Taha AE, Tiwari R, Yatoo MI, Bhatt P, Khurana SK, Dhama K. Omega-3 and omega-6 fatty acids in poultry nutrition: effect on production performance and health. Animals. 2019;9(8):19. PubMed PMC

Ambati RR, Gogisetty D, Aswathanarayana RG, Ravi S, Bikkina PN, Bo L, Yuepeng S. Industrial potential of carotenoid pigments from microalgae: current trends and future prospects. Crit Rev Food Sci Nutr. 2019;59(12):1880–1902. doi: 10.1080/10408398.2018.1432561. PubMed DOI

Balk EM, Lichtenstein AH, Chung M, Kupelnick B, Chew P, Lau J. Effects of omega-3 fatty acids on serum markers of cardiovascular disease risk: a systematic review. Atherosclerosis. 2006;189(1):19–30. doi: 10.1016/j.atherosclerosis.2006.02.012. PubMed DOI

Bean LD, Leeson S. Long-term effects of feeding flaxseed on performance and egg fatty acid composition of brown and white hens. Poult Sci. 2003;82(3):388–394. doi: 10.1093/ps/82.3.388. PubMed DOI

Cepák V, Přibyl P, Kohoutková J, Kaštánek P. Optimization of cultivation conditions for fatty acid composition and EPA production in the eustigmatophycean microalga Trachydiscus minutus. J Appl Phycol. 2014;26(1):181–190. doi: 10.1007/s10811-013-0119-z. DOI

Cha KH, Lee HJ, Koo SY, Song DG, Lee DU, Pan CH. Optimization of pressurized liquid extraction of carotenoids and chlorophylls from Chlorella vulgaris. J Agric Food Chem. 2010;58(2):793–797. doi: 10.1021/jf902628j. PubMed DOI

de Lange LLM, Elferink GO, Nollet L. Producing selenium enriched eggs by different Se-sources in the feed. Beekbergen: World's Poultry Science Association (WPSA); 2005. pp. 525–528.

Fisinin VI, Papazyan TT, Surai PE. Producing selenium-enriched eggs and meat to improve the selenium status of the general population. Crit Rev Biotechnol. 2009;29(1):18–28. doi: 10.1080/07388550802658030. PubMed DOI

Fraeye I, Bruneel C, Lemahieu C, Buyse J, Muylaert K, Foubert I. Dietary enrichment of eggs with omega-3 fatty acids: A review. Food Res Int. 2012;48(2):961–969. doi: 10.1016/j.foodres.2012.03.014. DOI

Fredriksson S, Elwinger K, Pickova J. Fatty acid and carotenoid composition of egg yolk as an effect of microalgae addition to feed formula for laying hens. Food Chem. 2006;99(3):530–537. doi: 10.1016/j.foodchem.2005.08.018. DOI

Gong M, Bassi A. Carotenoids from microalgae: a review of recent developments. Biotechnol Adv. 2016;34(8):1396–1412. doi: 10.1016/j.biotechadv.2016.10.005. PubMed DOI

Hooper L, Thompson RL, Harrison RA, Summerbell CD, Ness AR, Moore H, Worthington HV, Durrington PN, Higgins JPT, Capps NE, Riemersma RA, Ebrahim SB, Smith GD. Risks and benefits of omega 3 fats for mortality, cardiovascular disease, and cancer: systematic review. Br Med J. 2006;332(7544):752–755. doi: 10.1136/bmj.38755.366331.2F. PubMed DOI PMC

Humhal T, Kastanek P, Jezkova Z, Cadkova A, Kohoutkova J, Branyik T. Use of saline waste water from demineralization of cheese whey for cultivation of Schizochytrium limacinum PA-968 and Japonochytrium marinum AN-4. Bioprocess Biosyst Eng. 2017;40(3):395–402. doi: 10.1007/s00449-016-1707-5. PubMed DOI

Lemahieu C, Bruneel C, Termote-Verhalle R, Muylaert K, Buyse J, Foubert I. Impact of feed supplementation with different omega-3 rich microalgae species on enrichment of eggs of laying hens. Food Chem. 2013;141(4):4051–4059. doi: 10.1016/j.foodchem.2013.06.078. PubMed DOI

Lemahieu C, Bruneel C, Termote-Verhalle R, Muylaert K, Foubert I, Buyse J. Dynamics of omega-3 long chain polyunsaturated fatty acid incorporation in egg yolk by autotrophic microalgal supplementation. Eur J Lipid Sci Technol. 2015;117(9):1391–1397. doi: 10.1002/ejlt.201400473. DOI

Martins DA, Custodio L, Barreira L, Pereira H, Ben-Hamadou R, Varela J, Abu-Salah KM. Alternative sources of n-3 long-chain polyunsaturated fatty acids in marine microalgae. Mar Drugs. 2013;11(7):2259–2281. doi: 10.3390/md11072259. PubMed DOI PMC

Matos J, Cardoso C, Bandarra NM, Afonso C. Microalgae as healthy ingredients for functional food: a review. Food Funct. 2017;8(8):2672–2685. doi: 10.1039/C7FO00409E. PubMed DOI

Mesías FJ, Martínez-Carrasco F, Martínez JM, Gaspar P. Functional and organic eggs as an alternative to conventional production: a conjoint analysis of consumers' preferences. J Sci Food Agric. 2011;91(3):532–538. doi: 10.1002/jsfa.4217. PubMed DOI

Patias LD, Fernandes AS, Petry FC, Mercadante AZ, Jacob-Lopes E, Zepka LQ. Carotenoid profile of three microalgae/cyanobacteria species with peroxyl radical scavenger capacity. Food Res Int. 2017;100:260–266. doi: 10.1016/j.foodres.2017.06.069. PubMed DOI

Payne RL, Lavergne TK, Southern LL. Effect of inorganic versus organic selenium on hen production and egg selenium concentration. Poult Sci. 2005;84(2):232–237. doi: 10.1093/ps/84.2.232. PubMed DOI

Petkov G, Garcia G. Which are fatty acids of the green alga Chlorella? Biochem Syst Ecol. 2007;35(5):281–285. doi: 10.1016/j.bse.2006.10.017. DOI

Pribyl P, Cepak V, Kastanek P, Zachleder V. Elevated production of carotenoids by a new isolate of Scenedesmus sp. Algal Res. 2015;11:22–27. doi: 10.1016/j.algal.2015.05.020. DOI

Ramesh Kumar B, Deviram G, Mathimani T, Duc PA, Pugazhendhi A. Microalgae as rich source of polyunsaturated fatty acids. Biocatal Agric Biotechnol. 2019;17:583–588. doi: 10.1016/j.bcab.2019.01.017. DOI

Rezanka T, Petrankova M, Cepak V, Pribyl P, Sigler K, Cajthaml T. Trachydiscus minutus, a new biotechnological source of eicosapentaenoic acid. Folia Microbiol. 2010;55(3):265–269. doi: 10.1007/s12223-010-0039-0. PubMed DOI

Rizzi L, Bochicchio D, Bargellini A, Parazza P, Simioli M. Effects of dietary microalgae, other lipid sources, inorganic selenium and iodine on yolk n-3 fatty acid composition, selenium content and quality of eggs in laying hens. J Sci Food Agric. 2009;89(10):1775–1781. doi: 10.1002/jsfa.3655. DOI

Ruxton CHS. The nutritional properties and health benefits of eggs. Food Sci Nutr. 2010;40(3):263–279. doi: 10.1108/00346651011043961. DOI

Schlatterer J, Breithaupt DE. Xanthophylls in commercial egg yolks: quantification and identification by HPLC and LC-(APCI)MS using a C30 phase. J Agric Food Chem. 2006;54(6):2267–2273. doi: 10.1021/jf053204d. PubMed DOI

Skrivan M, Simane J, Dlouha G, Doucha J. Effect of dietary sodium selenite, Se-enriched yeast and Se-enriched Chlorella on egg Se concentration, physical parameters of eggs and laying hen production. Czech J Anim Sci. 2006;51(4):163–167. doi: 10.17221/3924-CJAS. DOI

Sparks NHC. The hen’s egg – is its role in human nutrition changing? Worlds Poult Sci J. 2007;62(2):308–315. doi: 10.1079/WPS200599. DOI

Stark KD, Van Elswyk ME, Higgins MR, Weatherford CA, Salem N. Global survey of the omega-3 fatty acids, docosahexaenoic acid and eicosapentaenoic acid in the blood stream of healthy adults. Prog Lipid Res. 2016;63:132–152. doi: 10.1016/j.plipres.2016.05.001. PubMed DOI

Steinrucken P, Erga SR, Mjos SA, Kleivdal H, Prestegard SK. Bioprospecting North Atlantic microalgae with fast growth and high polyunsaturated fatty acid (PUFA) content for microalgae-based technologies. Algal Res. 2017;26:392–401. doi: 10.1016/j.algal.2017.07.030. PubMed DOI PMC

Sun X, Zhong Y, Huang Z, Yang Y. Selenium accumulation in unicellular green alga Chlorella vulgaris and its effects on antioxidant enzymes and content of photosynthetic pigments. PLoS One. 2014;9(11):e112270. doi: 10.1371/journal.pone.0112270. PubMed DOI PMC

Surai PF, Sparks NHC. Designer eggs: from improvement of egg composition to functional food. Trends Food Sci Technol. 2001;12(1):7–16. doi: 10.1016/S0924-2244(01)00048-6. DOI

Utterback PL, Parsons CM, Yoon I, Butler J. Effect of supplementing selenium yeast in diets of laying hens on egg selenium content. Poult Sci. 2005;84(12):1900–1901. doi: 10.1093/ps/84.12.1900. PubMed DOI

Zaheer K. An updated review on chicken eggs: production, consumption, management aspects and nutritional benefits to human health. Food Sci Nutr. 2015;6(13):13.

Zhang J, Sun Z, Sun PP, Chen TP, Chen F. Microalgal carotenoids: beneficial effects and potential in human health. Food Funct. 2014;5(3):413–425. doi: 10.1039/c3fo60607d. PubMed DOI